Oxidative stress and life histories: unresolved issues and current needs

John R Speakman, Jonathan D Blount, Anne M Bronikowski, Rochelle Buffenstein, Caroline Isaksson, Tom B L Kirkwood, Pat Monaghan, Susan E Ozanne, Michaël Beaulieu, Michael Briga, Sarah K Carr, Louise L Christensen, Helena M Cochemé, Dominic L Cram, Ben Dantzer, Jim M Harper, Diana Jurk, Annette King, Jose C Noguera, Karine SalinElin Sild, Mirre J P Simons, Shona Smith, Antoine Stier, Michael Tobler, Emma Vitikainen, Malcolm Peaker, Colin Selman

Research output: Contribution to journalArticle

90 Citations (Scopus)
4 Downloads (Pure)

Abstract

Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.

Original languageEnglish
Pages (from-to)5745-5757
Number of pages13
JournalEcology and Evolution
Volume5
Issue number24
Early online date17 Nov 2015
DOIs
Publication statusPublished - Dec 2015

Fingerprint

life history
oxidative stress
life history theory
physiology
need
stress measurement
free radical
prediction
repair
wild animals
testing
damage

Keywords

  • aging
  • disposable soma theory
  • free radicals
  • life-history theory
  • oxidative stress

Cite this

Speakman, J. R., Blount, J. D., Bronikowski, A. M., Buffenstein, R., Isaksson, C., Kirkwood, T. B. L., ... Selman, C. (2015). Oxidative stress and life histories: unresolved issues and current needs. Ecology and Evolution, 5(24), 5745-5757. https://doi.org/10.1002/ece3.1790

Oxidative stress and life histories : unresolved issues and current needs. / Speakman, John R; Blount, Jonathan D; Bronikowski, Anne M; Buffenstein, Rochelle; Isaksson, Caroline; Kirkwood, Tom B L; Monaghan, Pat; Ozanne, Susan E; Beaulieu, Michaël; Briga, Michael; Carr, Sarah K; Christensen, Louise L; Cochemé, Helena M; Cram, Dominic L; Dantzer, Ben; Harper, Jim M; Jurk, Diana; King, Annette; Noguera, Jose C; Salin, Karine; Sild, Elin; Simons, Mirre J P; Smith, Shona; Stier, Antoine; Tobler, Michael; Vitikainen, Emma; Peaker, Malcolm; Selman, Colin.

In: Ecology and Evolution, Vol. 5, No. 24, 12.2015, p. 5745-5757.

Research output: Contribution to journalArticle

Speakman, JR, Blount, JD, Bronikowski, AM, Buffenstein, R, Isaksson, C, Kirkwood, TBL, Monaghan, P, Ozanne, SE, Beaulieu, M, Briga, M, Carr, SK, Christensen, LL, Cochemé, HM, Cram, DL, Dantzer, B, Harper, JM, Jurk, D, King, A, Noguera, JC, Salin, K, Sild, E, Simons, MJP, Smith, S, Stier, A, Tobler, M, Vitikainen, E, Peaker, M & Selman, C 2015, 'Oxidative stress and life histories: unresolved issues and current needs', Ecology and Evolution, vol. 5, no. 24, pp. 5745-5757. https://doi.org/10.1002/ece3.1790
Speakman JR, Blount JD, Bronikowski AM, Buffenstein R, Isaksson C, Kirkwood TBL et al. Oxidative stress and life histories: unresolved issues and current needs. Ecology and Evolution. 2015 Dec;5(24):5745-5757. https://doi.org/10.1002/ece3.1790
Speakman, John R ; Blount, Jonathan D ; Bronikowski, Anne M ; Buffenstein, Rochelle ; Isaksson, Caroline ; Kirkwood, Tom B L ; Monaghan, Pat ; Ozanne, Susan E ; Beaulieu, Michaël ; Briga, Michael ; Carr, Sarah K ; Christensen, Louise L ; Cochemé, Helena M ; Cram, Dominic L ; Dantzer, Ben ; Harper, Jim M ; Jurk, Diana ; King, Annette ; Noguera, Jose C ; Salin, Karine ; Sild, Elin ; Simons, Mirre J P ; Smith, Shona ; Stier, Antoine ; Tobler, Michael ; Vitikainen, Emma ; Peaker, Malcolm ; Selman, Colin. / Oxidative stress and life histories : unresolved issues and current needs. In: Ecology and Evolution. 2015 ; Vol. 5, No. 24. pp. 5745-5757.
@article{58764188a89f4c21ba4ea8c015486e5e,
title = "Oxidative stress and life histories: unresolved issues and current needs",
abstract = "Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.",
keywords = "aging, disposable soma theory, free radicals, life-history theory, oxidative stress",
author = "Speakman, {John R} and Blount, {Jonathan D} and Bronikowski, {Anne M} and Rochelle Buffenstein and Caroline Isaksson and Kirkwood, {Tom B L} and Pat Monaghan and Ozanne, {Susan E} and Micha{\"e}l Beaulieu and Michael Briga and Carr, {Sarah K} and Christensen, {Louise L} and Cochem{\'e}, {Helena M} and Cram, {Dominic L} and Ben Dantzer and Harper, {Jim M} and Diana Jurk and Annette King and Noguera, {Jose C} and Karine Salin and Elin Sild and Simons, {Mirre J P} and Shona Smith and Antoine Stier and Michael Tobler and Emma Vitikainen and Malcolm Peaker and Colin Selman",
note = "Funded by Rank Prize Funds Acknowledgments This study was the result of a week-long workshop sponsored by the Rank prize funds attended by all the authors. We are grateful to the Rank prize funds for supporting this meeting.",
year = "2015",
month = "12",
doi = "10.1002/ece3.1790",
language = "English",
volume = "5",
pages = "5745--5757",
journal = "Ecology and Evolution",
issn = "2045-7758",
publisher = "Wiley",
number = "24",

}

TY - JOUR

T1 - Oxidative stress and life histories

T2 - unresolved issues and current needs

AU - Speakman, John R

AU - Blount, Jonathan D

AU - Bronikowski, Anne M

AU - Buffenstein, Rochelle

AU - Isaksson, Caroline

AU - Kirkwood, Tom B L

AU - Monaghan, Pat

AU - Ozanne, Susan E

AU - Beaulieu, Michaël

AU - Briga, Michael

AU - Carr, Sarah K

AU - Christensen, Louise L

AU - Cochemé, Helena M

AU - Cram, Dominic L

AU - Dantzer, Ben

AU - Harper, Jim M

AU - Jurk, Diana

AU - King, Annette

AU - Noguera, Jose C

AU - Salin, Karine

AU - Sild, Elin

AU - Simons, Mirre J P

AU - Smith, Shona

AU - Stier, Antoine

AU - Tobler, Michael

AU - Vitikainen, Emma

AU - Peaker, Malcolm

AU - Selman, Colin

N1 - Funded by Rank Prize Funds Acknowledgments This study was the result of a week-long workshop sponsored by the Rank prize funds attended by all the authors. We are grateful to the Rank prize funds for supporting this meeting.

PY - 2015/12

Y1 - 2015/12

N2 - Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.

AB - Life-history theory concerns the trade-offs that mold the patterns of investment by animals between reproduction, growth, and survival. It is widely recognized that physiology plays a role in the mediation of life-history trade-offs, but the details remain obscure. As life-history theory concerns aspects of investment in the soma that influence survival, understanding the physiological basis of life histories is related, but not identical, to understanding the process of aging. One idea from the field of aging that has gained considerable traction in the area of life histories is that life-history trade-offs may be mediated by free radical production and oxidative stress. We outline here developments in this field and summarize a number of important unresolved issues that may guide future research efforts. The issues are as follows. First, different tissues and macromolecular targets of oxidative stress respond differently during reproduction. The functional significance of these changes, however, remains uncertain. Consequently there is a need for studies that link oxidative stress measurements to functional outcomes, such as survival. Second, measurements of oxidative stress are often highly invasive or terminal. Terminal studies of oxidative stress in wild animals, where detailed life-history information is available, cannot generally be performed without compromising the aims of the studies that generated the life-history data. There is a need therefore for novel non-invasive measurements of multi-tissue oxidative stress. Third, laboratory studies provide unrivaled opportunities for experimental manipulation but may fail to expose the physiology underpinning life-history effects, because of the benign laboratory environment. Fourth, the idea that oxidative stress might underlie life-history trade-offs does not make specific enough predictions that are amenable to testing. Moreover, there is a paucity of good alternative theoretical models on which contrasting predictions might be based. Fifth, there is an enormous diversity of life-history variation to test the idea that oxidative stress may be a key mediator. So far we have only scratched the surface. Broadening the scope may reveal new strategies linked to the processes of oxidative damage and repair. Finally, understanding the trade-offs in life histories and understanding the process of aging are related but not identical questions. Scientists inhabiting these two spheres of activity seldom collide, yet they have much to learn from each other.

KW - aging

KW - disposable soma theory

KW - free radicals

KW - life-history theory

KW - oxidative stress

U2 - 10.1002/ece3.1790

DO - 10.1002/ece3.1790

M3 - Article

C2 - 26811750

VL - 5

SP - 5745

EP - 5757

JO - Ecology and Evolution

JF - Ecology and Evolution

SN - 2045-7758

IS - 24

ER -